Elements of a neurobiological theory of the hippocampus: The role of activity-dependent synaptic plasticity in memory

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 358, Issue 1432, 2003, Pages 773-786

  Morris, R G M ^a   Moser, E I ^b   Riedel, G ^c   Martin, S J ^a   Sandin, J ^d   Day, M ^a,e   O'Carroll, C ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d KAROLINSKA INSTITUTE   (Sweden)

^e GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Early long term potentiation; Event memory; Late long term potentiation; Memory consolidation; Synaptic plasticity; Synaptic tagging

Indexed keywords

MEMORY; NEUROLOGY;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0038561176     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2002.1264     Document Type: Article

References (107)

1. Abraham, W. C. 2003 How long will long-term potentiation last? Phil. Trans. R. Soc. Lond. B 358, 735-744. (DOI 10.1098/rstb.2002.1222.)
2. Aggleton, J. P. & Brown, M. W. 1999 Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav. Brain Sci. 22, 425-489.
3. Aggleton, J. P. & Pearce, J. M. 2001 Neural systems underlying episodic memory: insights from animal research. Phil. Trans. R. Soc. Lond. B 356, 1467-1482. (DOI 10.1098/rstb.2001.0946.)
4. Amaral, D. G. 1990 Neurons, numbers and the hippocampal network. In Progress in brain research (ed. J. Storm-Mathisen, J. Zimmer & O. P. Ottersen), pp. 1-11. Amsterdam, The Netherlands: Elsevier.
5. Amaral, D. G. & Witter, M. P. 1989 The three dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591.
6. Barco, A., Alarcon, J. M. & Kandel, E. R. 2002 Expression of a constitutively active CREB protein facilitates the late phase of long-term potentiation by enhancing synaptic capture. Cell 108, 689-703.
7. Bartlett, F. C. 1932 Remembering. Cambridge University, Press.
8. Belvin, M. P. & Yin, J. C. 1997 Drosophila learning and memory: recent progress and new approaches. Bioessays 19, 1083-1089.
9. Bliss, T. V. P. & Collingridge, G. L. 1993 A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
10. Bliss, T. V. P. & Lømo, T. 1973 Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 331-356.
11. Bransford, J. D. 1979 Human cognition: learning, understanding and remembering. Belmont, CA: Wadsworth.
12. Brown, M. W. & Aggleton, J. P. 2001 Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Trends Cogn. Sci, 2, 51-61.
13. Brun, V. H., Ytterbo, K., Morris, R. G., Moser, M. B. & Moser, E. I. 2001 Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation. J. Neurosci. 21, 356-362.
14. Brun, V. H., Omass, M. K., Molden, S., Steffenach, H. A., Witter, M. P., Moser, M.-B. & Moser, E. I. 2002 Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246.
15. Buszaki, G. 1989 Two-stage model of memory-trace formation: a role for 'noisy' brain states. Neuroscience 31, 551-570.
16. Clayton, N. S. & Dickinson, A. 1998 What, where and when: episodic-like memory during cache recovery by scrub jays. Nature 395, 272-274.
17. Davis, H. P. & Squire, L. R. 1984 Protein synthesis and memory: a review. Psychol. Bull. 96, 518-559.
18. Day, M. & Morris, R. G. M. 2001 Memory consolidation and NMDA receptors: discrepancy between genetic and pharmacological approaches. Science 293, 755.
19. Day, M. & Morris, R. G. M. 2003 Episodic-like memory in the rat: glutamate receptor-dependent encoding and recall of one-trial paired-associate learning. (Submitted.)
20. Dudai, Y. & Morris, R. G. M. 2001 To consolidate or not to consolidate: what are the questions? In Brain, perception and memory: advances in cognitive sciences (ed. J. Bolhuis), pp. 147-162. Oxford University, Press.
21. Duzel, E., Vargha-Khadem, F., Heinze, H. J. & Mishkin, M. 2001 Brain activity, evidence for recognition without recollection after early hippocampal damage. Proc. Natl Acad. Sci. USA 98, 8101-8106.
22. Eichenbaum, H. & Cohen, N. J. 2001 From conditioning to conscious recollection. New York: Oxford University Press.
23. Frank, L. M., Brown, E. N. & Wilson, M. 2000 Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27, 169-178.
24. Frey, U. & Morris, R. G. M. 1997 Synaptic tagging and long-term potentiation. Nature 385, 533-536.
25. Frey, U. & Morris, R. G. M. 1998a Weak before strong: dissociating synaptic-tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37, 545-552.
26. Frey, U. & Morris, R. G. M. 1998b Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21, 181-188.
27. Frey, U., Matthies, H., Reymann, K. G. & Matthies, H. 1991 The effect of dopaminergic d1-receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci. Lett. 129, 111-114.
28. Fyhn, M., Molden, S., Hollup, S. A., Moser, M.-B. & Moser, E. I. 2002 Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35, 555-566.
29. Gaffan, D. 1994 Scene-specific memory for objects: a model of episodic memory impairment in monkeys with fornix transection. J. Cogn. Neurosci. 6, 305-320.
30. Gaffan, D. 2001 What is a memory system? Horel's critique revisited Behav. Brain Res. 127, 5-11.
31. Goelet, P., Castellucci, V. F., Schacher, S. & Kandel, E. R. 1986 The long and the short of long-term memory - a molecular framework. Nature 322, 419-422.
32. Golding, N. L. & Spruston, N. 1998 Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21, 1189-1200.
33. Golding, N. L., Staff, N. P. & Spruston, N. 2002 Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331.
34. Griffiths, D., Dickinson, A. & Clayton, N. 1999 Episodic memory: what can animals remember about their past? Trends Cogn. Sci. 3, 74-80.
35. Grimwood, P. D., Martin, S. J. & Morris, R. G. M. 2001 Synaptic plasticity and memory. In Synapses (ed. W. M. Cowan, T. C. Sudhof & C. F. Stevens), pp. 519-570. Baltimore, MD: Johns Hopkins University Press.
36. Hédou, G. & Mansuy, I. M. 2003 Inducible molecular switches for the study of long-term potentiation. Phil. Trans. R. Soc. Lond. B 358, 797-804. (DOI 10.1098/rstb.2002.1245.)
37. Hill, A. J. 1978 First occurrence of hippocampal spatial firing in a new environment. Exp. Neurol. 62, 282-297.
38. Hoffman, K. L. & McNaughton, B. L. 2002 Sleep on it: cortical reorganization after-the-fact. Trends Neurosci. 25, 1-2.
39. Izquierdo, I. & Medina, J. H. 1995 Correlation between the pharmacology of long-term potentiation and the pharmacology of memory. Neurobiol. Learning Memory 63, 19-32.
40. Izquierdo, I. & Medina, J. H. 1998 On brain lesions, the milkman and Sigmunda. Trends Neurosci. 21, 423-426.
41. Jeffery, K. J. 1997 LTP and spatial learning: where to next? Hippocampus 7, 95-110.
42. Kandel, E. R. & Schwartz, J. H. 1982 Molecular biology of learning: modulation of transmitter release. Science 218, 433-443.
43. Kapur, N. 1999 Syndromes of retrograde amnesia: a conceptual and empirical synthesis. Psychol. Bull. 125, 800-825.
44. Kentros, C., Hargreaves, E., Hawkins, R. D., Kandel, E. R., Shapiro, M. & Muller, R. V. 1998 Abolition of long-term stability of new hippocampal place cell maps by NMDA receptor blockade. Science 280, 2121-2126.
45. King, C., Henze, D. A., Leinekugel, X. & Buzsaki, G. 1999 Hebbian modification of a hippocampal population pattern in the rat. J. Physiol. 521, 159-167.
46. Krug, M., Lossner, B. & Ott, T. 1984 Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res. Bull. 13, 39-42.
47. Lever, C., Wills, T., Cacucci, F., Burgess, N. & O'Keefe, J. 2002 Long-term plasticity in hippocampal place-cell representation of environmental geometry. Nature 416, 90-94.
48. Louie, K. & Wilson, M. A. 2001 Temporally structured REM sleep replay of awake hippocampal ensemble activity. Neuron 29, 145-156.
49. Lynch, G. 2003 Long-term potentiation in the Eocene. Phil. Trans. R. Soc. Lond. B 358, 625-628. (DOI 10.1098/rstb.2002.1253.)
50. Lynch, G. & Faudry, M. 1984 The biochemistry of memory: a new and specific hypothesis. Science 224, 1057-1063.
51. McClelland, J. L., McNaughton, B. L. & O'Reilly, R. C. 1995 Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419-457.
52. McGaugh, J. L. 2000 Memory: a century of consolidation. Science 287, 248-251.
53. McHugh, T. J., Blum, K. I., Tsien, J. Z., Tonegawa, S. & Wilson, M. A. 1996 Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice. Cell 87, 1339-1349.
54. McNaughton, B. L. & Barnes, C. A. 1986 Long-term enhancement of hippocampal synaptic transmission and the acquisition of spatial information. J. Neurosci. 6, 563-571.
55. McNaughton, B. L. & Morris, R. G. M. 1987 Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408-415.
56. McNaughton, B. L., Barnes, C. A., Meltzer, J. & Sutherland, R. J. 1989 Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp. Brain Res. 76, 485-496.
57. McNaughton, B. L. (and 12 others) 2003 Off-line reprocessing of recent memory and its role in memory consolidation: a progress report. In Sleep and synaptic plasticity (ed. C. Smith & P. Maquet), pp. 225-246. Oxford University Press.
58. Maguire, E. A., Vargha-Khadem, F. & Mishkin, M. 2001 The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124, 1156-1170.
59. Maren, S. & Baudry, M. 1995 Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiol. Learning Memory 63, 1-18.
60. Marr, D. 1971 Simple memory: a theory for archicortex. Phil. Trans. R. Soc. Lond. B 262, 23-81.
61. Martin, S. J. & Morris, R. G. M. 2002 New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus 12, 609-636.
62. Martin, S. J., Grimwood, P. D. & Morris, R. G. 2000 Synaptic plasticity and memory: an evaluation of the hypothesis. A. Rev. Neurosci. 23, 649-711.
63. Mishkin, M., Suzuki, W. A., Gadian, D. G. & Vargha-Khadem, F. 1997 Hierarchical organization of cognitive memory. Phil. Trans. R. Soc. Lond. B 352, 1461-1467. (DOI 10.1098/rst:b.1997.0132.)
64. Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R. & Schacher, S. 1986 A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234, 1249-1254.
65. Morris, R. G. M. 2001 Episodic-like memory in animals: psychological criteria, neural mechanisms and the value of episodic-like tasks to investigate animal models of neurodegenerative disease. Phil. Trans. R. Soc. Lond. B 356, 1453-1465. (DOI 10.1098/rstb.2001.0945.)
66. Morris, R. G. M. & Frey, U. 1997 Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Phil. Trans. R. Soc. Lond. B 352, 1489-1503. (DOI 10.1098/rstb.1997.0136.)
67. Morris, R. G. M., Anderson, E., Lynch, G. S. & Baudry, M. 1986 Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319, 774-776.
68. Moscovitch, M. 1995 Recovered consciousness: a hypothesis concerning modularity and episodic memory. J. Clin. Exp. Neuropsychol. 17, 276-290.
69. Moser, E. I., Krobert, K. A., Moser, M. B. & Morris, R. G. M. 1998 Impaired spatial learning after saturation of long-term potentiation. Science 281, 2038-2042.
70. Nadel, L. & Moscovitch, M. 1997 Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217-227.
71. Nakazawa, K. (and 10 others) 2002 Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211-218.
72. O'Keefe, J. & Dostrovsky, J. 1971 The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171-175.
73. O'Keefe, J. & Nadel, L. 1978 The hippocampus as a cognitive map. Oxford: Clarendon.
74. O'Reilly, R. C. & Rudy, J. W. 2001 Conjunctive representations in learning and memory: principles of cortical and hippocampal function. Psychol. Rev. 108, 311-345.
75. Packard, M. G. & Teather, L. A. 1997 Double-dissociation of hippocampal and dorsal-striatal memory systems by post-training intracerebral injections of 2-amino-5-phsophonopentanoic acid. Behav. Neurosci. 111, 543-551.
76. Paulsen, O. & Moser, E. I. 1998 A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21, 273-278.
77. Pittenger, C. & Kandel, E. R. 2003 In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Phil. Trans. R. Soc. Lond. B 358, 757-763. (DOI 10.1098/rstb.2002.1247.)
78. Quirk, G. J., Muller, R. U., Kubie, J. L. & Ranck, J. B. 1992 The positional firing properties of medial entorhinal neurons: descriiption and comparison with hippocampal place cells. J. Neurosci. 12, 1945-1963.
79. Riedel, G., Micheau, J., Lam, A. G. M., Roloff, E. V. L., Martin, S. J., Bridge, H., de Hoz, L., Poeschel, B., McCulloch, J. & Morris, R. G. M. 1999 Reversible neural inactivation reveals hippocampal participation in several memory processes. Nature Neurosci. 2, 898-905.
80. Riedel, G., Platt, B. & Micheau, J. 2003 Glutamate receptor function in learning and memory. Behav. Brain Res. (In the press.)
81. Rioult-Pedotti, M.-S., Friedman, D. & Donoghue, J. P. 2000 Learning-induced LTP in neocortex. Science 290, 533-536.
82. Rolls, E. T. & Treves, A. 1998 Neural networks and brain function. Oxford University Press.
83. Rose, S. P. R. 1995 Glycoproteins and memory formation. Behav. Brain Formation 66, 73-78.
84. Rotenberg, A., Mayford, M., Hawkins, R. D., Kandel, E. R. & Muller, R. U. 1996 Mice expressing activated CaMKII lack low frequency LTP and do not form stable place cells in the CA1 region of the hippocampus. Cell 87, 1351-1361.
85. Rotenberg, A., Abel, T., Hawkins, R. D., Kandel, E. R. & Muller, R. U. 2000 Parallel instabilities of long-term potentiation, place cells, and learning caused by decreased protein kinase A activity. J. Neurosci. 20, 8096-8102.
86. Shimizu, E., Tang, Y. P., Rampon, C. & Tsien, J. Z. 2000 NMDA receptor-dependent synaptic reinforcement as a crucial process for memory consolidation. Science 290, 1170-1174.
87. Silva, A. J., Stevens, C. F., Tonegawa, S. & Wang, Y. 1992 Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 257, 201-206.
88. Squire, L. R. 1992 Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195-231.
89. Squire, L. R. & Zola-Morgan, S. 1991 The primate hippocampal formation: evidence for a time-limited role in memory storage. Science 253, 1380-1386.
90. Steele, R. J. & Morris, R. G. M. 1999 Delay-dependent impairment of a matching-to-place task with chronic and intrahippocampal infusion of the NMDA-antagonist D-AP5. Hippocampus 9, 118-136.
91. Steffenach, H. A., Sloviter, R. S., Moser, E. I. & Moser, M. B. 2002 Impaired retention of spatial memory after transection of longitudinally oriented axons of hippocampal CA3 pyramidal cells. Proc. Natl Acad. Sci. USA 99, 3194-3198.
92. Stevens, C. F. 1998 A million dollar question: does LTP = memory? Neuron 20, 1-2.
93. Sutherland, R. J. & Rudy, J. W. 1989 Confugural association theory: the role of the hippocampal formation in learning, memory, and amnesia. Psychobiol. 17, 129-144.
94. Swanson-Park, J. L., Coussens, C. M., Mason-Parker, S. E., Raymond, C. R., Hargreaves, E. L., Dragunow, M., Cohen, A. S. & Abraham, W. C. 1999 A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92, 485-497.
95. Teyler, T. J. & Discenna, P. 1984 Long-term potentiation as a candidate mnemonic device. Brain Res. Rev. 7, 15-28.
96. Teyler, T. J. & Discenna, P. 1987 Long-term potentiation. A. Rev. Neurosci. 10, 131-161.
97. Thompson, L. T. & Best, P. J. 1990 Long-term stability of the place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 509, 299-308.
98. Tonegawa, S., Nakazawa, K. & Wilson, M. A. 2003 Genetic neuroscience of mammalian learning and memory. Phil. Trans. R. Soc. Lond. B 358, 787-795. (DOI 10.1098/rstb.2002.1243.)
99. Tulving, E. 1983 Elements of episodic memory. Oxford: Clarendon.
100. Turrigiano, G., Leslie, K. R., Desai, N., Rutherford, L. C. & Nelson, S. 1998 Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-895.
101. Vargha-Khadem, F., Gadian, D. G., Watkins, K. E., Connely, A., Van Paesschen, W. & Mishkin, M. 1997 Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376-380.
102. Vargha-Khadem, F., Gadian, D. G. & Mishkin, M. 2001 Dissociations in cognitive memory: the syndrome of developmental amnesia. Phil. Trans. R. Soc. Lond. B 356, 1435-1440.
103. Villarreal, D. M., Do, V., Haddad, E. & Derrick, B. E. 2002 NMDA receptor antagonists sustain LTP and spatial memory: active processes mediate LTP decay. Nature Neurosci. 5, 48-52.
104. Wigstrom, H. & Gustafsson, B. 1983 Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301, 603-604.
105. Willshaw, D. & Dayan, P. 1990 Optimal plasticity from matrix memories: what goes up must come down. Neural Commun. 2, 85-93.
106. Wilson, M. A. & McNaughton, B. L. 1993 Dynamics of the hippocampal ensemble code for space. Science 261, 1055-1058.
107. Wilson, M. A. & McNaughton, B. L. 1994 Reactivation of hippocampal ensemble memories during sleep. Science 265, 676-682.